DISTRIBUTION OF PHLEBOTOMINE SAND FLIES (DIPTERA:PSYCHODIDAE) IN LIMESTONE CAVES, KHAO PATHAWI, UTHAI THANI PROVINCE, THAILAND

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1 DISTRIBUTION OF PHLEBOTOMINE SAND FLIES (DIPTERA:PSYCHODIDAE) IN LIMESTONE CAVES, KHAO PATHAWI, UTHAI THANI PROVINCE, THAILAND R Polseela 1,2, A Vitta 1,2 and C Apiwathnasorn 3 1 Department of Microbiology and Parasitology, 2 Centre of Excellence in Medical Biotechnology, Faculty of Medical Science, Naresuan University, Phitsanulok, 3 Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand Abstract. This study investigated the species composition and density of the sand flies found inside four limestone caves at Khao Pathawi, Thap Than District, Uthai Thani Province. Sand flies were collected using Centers for Disease Control (CDC) light traps from October 2012 to September The sand flies were captured between 06:00 pm - 06:00 am. A total of 11,817 sand flies were collected with a male:female ratio of 1.0:1.2 (5,325:6,492). The specimens were identified as eight species belonging to three genera Phlebotomus, Sergentomyia, Chinius, and comprised of S. anodontis, P. argentipes, P. stantoni, S. barraudi, S. silvatica, S. gemmea, S. indica, and C. barbazani. Sergentomyia anodontis (55.0%) was the predominant species followed by P. argentipes (33.6%) and others. Five species of sand fly were found throughout the year in this area: P. argentipes, P. stantoni, S. anodontis, S. barraudi and S. gemmea. The highest average density of sand flies was found in Ratree cave (35.0 sand flies per trap per night) and lowest in Bandai cave (29.0 sand flies per trap per night). The population of sand fly fluctuated from the highest peak in December (28.5%) to the lowest peak in May (2.3%). The distribution of sand fly species in attraction areas is important for the control program of infection risk of leishmaniasis. Keywords: sand flies, CDC light traps, leishmaniasis, limestone cave, Thailand INTRODUCTION Leishmaniasis is a vector-borne disease caused by the protozoan parasite of Leishmania species. The parasite is transmitted by female sand flies, particu- Correspondence: R Polseela, Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok , Thailand. raxsinap@nu.ac.th,polseela@hotmail. com larly members of genera Lutzomyia and Phlebotomus. Phlebotomine sand flies (Diptera:Psychodidae) are found in a wide range of habitats. The genus Phlebotomus is responsible for the transmission of leishmaniasis in the Old World. About 40 species of Phlebotomus spp in the Old World have been proven or suspected to be vectors of Leishmania spp (Alexander and Maroli, 2003). Leishmania spp have a wide geographic distribution. Some species of sand flies are adapted to a range Vol 46 No. 3 May

Fig 2 Inside a limestone cave at Khao Pathawi, Thap Than, District, Uthai Thani Province. of environmental conditions with a wide distribution.

2 Southeast Asian J Trop Med Public Health Fig 1 Outside a limestone cave at Khao Pathawi, Thap Than District, Uthai Thani Province. Fig 1 Outside limestone caves in Khao Pattawee, Thap Than District, Uthai Thani Province. Fig 2 Inside limestone caves in Khao Pattawee, Thap Than, Uthai Thani Province. Fig 2 Inside a limestone cave at Khao Pathawi, Thap Than, District, Uthai Thani Province. of environmental conditions with a wide distribution. About 30 species of sand flies are proven vectors of at least 20 Leishmania species (Emamia and Yazdib, 2008). In Thailand, there are 5 genera (Phlebotomus, Sergentomyia, Idiophlebotomus, Chinius and Nemopalpus) including 27 species of sand flies reported from different habitats (Apiwathanasorn et al, 1989; 2011). Autochthonous cases of leishmaniasis are caused by Leishmania donovani, L. infantum and L. siamensis (Kongkaew et al, 2007; Maharom et al, 2008; Bualert et al, 2012). L. siamensis is a new species found in Thailand where it is the cause of visceral leishmaniasis (Sukmee et al, 2008; Bualert et al, 2012). P. argentipes is the species of sand flies involved in the transmission of leishmaniasis and it can be found in Thailand. At present, Sergentomyia gemmea may be a potential vector of L. siamensis which is the cause of visceral leishmaniasis in Thailand (Kanjanopas et al, 2013). The sand flies fauna is presented in different locations such as cave, forest, rural, urban, sylvatic and domestic areas (Magill et al, 1993). Previous studies have shown a diversity of sand flies in different parts of Thailand. Cave-dwelling phlebotomine sand flies are represented by different species in different sites (Polseela et al, 2007; 2011a,b; Shahar et al, 2011). The objective of this study was to determine the species composition and seasonal fluctuations of sand fly species inside caves within a single mountain region. This may assist in planning for programs of prevention and control of leishmaniasis. MATERIALS AND METHODS Study area The study collected sand flies from October 2012 to September 2013 from four limestone caves in Khao Pathawi, 426 Vol 46 No. 3 May 2015

3 Thap Than District, Uthai Thani Province: Ratree cave, Bandai cave, Aunag cave, and Phuttha Prawat cave. These caves situated on mountainsides at N, E (Figs 1 and 2). All caves are about m wide, m long and 5-30 m high. There are some birds and bats inside caves. The caves are surrounded by green trees and cover mainly by forest vegetation. The caves are near a village. In this area, measures of temperature and relative humidity were recorded monthly with a digital hygro-thermometer. The average temperature during the study were C. The annual average relative humidity is 54-94%. Rainfall data were provided by the Thai Meteorological Department. Sand fly collection and identification A survey of sand flies population was made using 32 miniature CDC light traps one night per month (Sudia and Chamberin,1962). CDC light traps were placed inside the cave at 5-8 m from each location. The trap were set near crack of rock. The traps were operated continuously for 12 hours (06:00 pm to 06:00 am) and the insects were collected after 12 hours period. During each month of survey in these caves, the sand flies were captured at the same site. The sand flies were separated from other arthropods under a stereo-microscope and stored in 80% alcohol for identification. Head and thorax of sand flies were separated and mounted with Hoyer s medium on glass slides. Taxonomic keys were used for identifications base on the morphology of female spermatheca, pharyngx, and male genitalia (Lewis, 1978). RESULTS Sand fly species composition and sex ratio A total of 11,817 phlebotomine sand flies were captured from the four caves. The highest peak of activity was found during December and then decreased to the lowest point in May (Tables 1 and 2). Eight species were identified of which 5 belonged to the genus Sergentomyia, 2 to the genus Phlebotomus, 1 to the genus Chinius (Table 2). The greatest number of specimens was collected in December, while P. argentipes, P. stantoni, S. barraudi, and S. anodontis were trapped throughout the whole year (Table 2). Both male and female flies were attracted by the light. The male to female ratio was 1.0:1.2 (6,492:5,325). The average density was sand flies per light trap per night. The highest average density was found in Ratree cave (35.05 sand flies per trap per night) and the lowest in Bandai cave (29.03 sand flies per trap per night). The known vector, P. argentipes had its peak in December (Fig 3). The monthly variation of sand fly density is presented in Fig 4. The minimum and maximum temperature and relative humidity values ranged between ºC, and 54-94%, respectively. DISCUSSION A survey of sand fly activity was conducted for a 12 month period inside four limestone caves using CDC light traps. The nocturnal activity among the different species of sand flies was studied (Apiwathnasorn et al, 1989, 1993; Polseela et al, 2007, 2011). The greatest numbers of specimens were collected in December. In this study, 8 species were identified: P.argentipes, P. stantoni, Sergentomyia anodontis, S. barraudi, S. silvatica, S. gemmea, S. indica, and Chinius barbazani. In Thailand, previous captures of sand flies documented 27 species (Apiwathnasorn et al, 1989; 1993; 2011). There are some Vol 46 No. 3 May

4 Southeast Asian J Trop Med Public Health Table 1 The number of sand flies captured by CDC light traps in limestone caves at Khao Pathawi, Thap Than District, Uthai Thani Province from October 2012 to September Cave Total % Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Bandai Male ,632 Female ,852 Total , Phuttha Prawat Male ,437 Female ,170 Total , Aunag Male ,011 Female ,191 Total , Ratree Female ,245 Male ,279 Total , , Total Female , , Male 987 1,083 1, , Total 1,565 2,013 3,373 1, , % Male:Female 1.0: Vol 46 No. 3 May 2015

5 Number of sand files 1,200 Fig 3 Nocturnal activity of Phlebotomus argentipes captured by CDC light traps in limestone caves at Khao Pathawi, Thap Than, Uthai Thani Province from October 2012 to September Number of sand files per trap night 1, Month Month Fig 4 Monthly variation of sand fly density captured by CDC light traps in limestone caves at Khao Pathawi, Thap Than, Uthai Thani Province from October 2012 to September species present in this area and others have disappeared, perhaps due to different environmental aspects in each area. S. barraudi was the most abundant species (55.0%). P. argentipes, a proven vector of Leishmania donovani, accounted for 33.6%. P. argentipes showed its highest peak in December. The greatest number of specimens was collected from a location near rock fissure in the cave. The density variation of sand fly observed in this study may indicate the present of sand flies to survive in the different caves. Sand flies in Phra Phothisat cave in Saraburi Province had their highest peak in July (436 sand flies per light trap per night) (Polseela et al, 2007). Currently there are two sand fly vectors of visceral leishmaniasis in other countries known in Thailand: P. argentipes and P. major major (Swaminath et al, 2006; Azizi et al, 2008). Of these, we found P. argentipes sand fly in this study. Thus a clear demarcation of the geographic limits of sand fly species and activity was demonstrated, according to the type of cave and different environments of this area. The findings also indicate a health risk for both locals and visitors to the caves in this area. Our previous study in Phra Phothisat cave and Tham Phra Pho Thisat Temple that had their highest peak in July and March (Polseela et al, 2007, 2011a). Thirteen species were found in Phra Phothisat cave, and 16 species were found in Tham Phra Pho Thisat Temple, Saraburi Province. There are some differences in the species composition found in difference area. P. argentipes was found at the level of % in Saraburi Province and 20.2% in Naresuan cave, Phitsanulok (Polseela et al, 2007; 2011a, b). In northern Israel, sand fly populations were prevalent from April to November and peaked between June and August (Kravchenko Vol 46 No. 3 May

6 Southeast Asian J Trop Med Public Health Table 2 The monthly distribution of sand flies species captured by CDC light in limestone caves at Khao Pathawi, Thap Than, Uthai Thani Province from October 2012 to September Species Total (%) Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep S.anodontis 829 1,187 1, ,493 (55.0) P.argentipes , ,971 (33.6) S.barraudi (5.0) S.gemmea (2.7) P.stantoni (2.2) S.silvatica (1.2) S.indica (0.3) C.barbazani (0.1) Total 1,565 2,013 3,373 1, ,817 (100.0) (%) (13.2) (17.0) (28.5) (12.7) (2.5) (3.6) (3.0) (2.3) (3.1) (3.2) (4.8) (6.1) (100.0) - et al, 2004). In January and February 2006, the sand fly was apparently absent in Saudi Arabia (Badry et al, 2008). Coleman et al (2006) reported sand fly activity periods in Iraq with the highest mean monthly captured rates in August, 2003 and July, Sand flies were active especially during the dry season (from May to November) in Marrakech, Morocco. The maximum of species richness was in May, when the daily temperature ranged between 13ºC and 26ºC. The species differed in their activity period; P. sergenti, was active especially during April, May and June (Boussaa et al, 2005). These seasonal patterns should be related to different environmental factors. Nocturnal activity of sand flies may result in transmitted pathogens to animals and humans. Those people living near the cave may be particularly at risk of exposure to such pathogens. Both sexes of the sand fly were found to have nocturnal activity in this study. The male to female ratio was 1.0:1.2. This suggests that both sexes of the sand fly are attracted to the light traps. Previous studies have shown the number of male sand flies captured using CDC light traps was significantly higher than that of female with a male:female ratio of 2.5:1 and 1.9:1 in Saraburi, Thailand (Polseela et al, 2007; 2011a). According to a study conducted in Cukurova plain, Turkey, males were found to be 4.7 times more abundant than females (Kasap et al, 2009). In different areas, the number of males captured was higher than that of females, with the sex ratio of 2.3:1 reported by Boussaa et al (2005), 3.4:1 by Hanafi et al (2007), 1.12:1 by Badry et al (2008) and 2:1 by Emamia and Yazdib (2008). The 430 Vol 46 No. 3 May 2015

7 higher proportion of males in the captures with CDC light traps could be explained by the natural behavior of the males to follow the females to assure fertilization during their displacements (Barata et al, 2004). Male sand flies have a weaker dispersal tendency than females and limit their flight to questing for food plants (Yuval and Schlein, 1986; Janini et al, 1995). The hopping behavior leads to the assumption that they do not disperse far from the breeding site (Killick-Kendrick, 1999). However, only the female sand fly can feed on blood and be the vector for leishmaniasis. For this study s month-by-month collection, the highest peak of capture was in December, and lowest in May. Temperature and humidity are factors closely related to duration of metamorphosis (Theodor, 1936). However, the optimum rearing temperatures differ among species of sand flies. Guernaoui et al (2006) reported that variations in the nocturnal activity rhythm are related to variations in temperature and relative humidity. The most favorable temperatures for development of sand flies are between 25 ºC and 30ºC (Safyanova, 1964). The activity of sand flies is continuous through the night and that relative humidity has a significant effect on the nocturnal activity. However, sand fly activity was closely related to climatic factors. Many investigations have demonstrated the existence of seasonal variations in the nocturnal activity of sand flies (Merrison et al, 1995; Polseela et al, 2011a). According to our findings, sand flies are active in the different caves. The high number of flies are found in several sites in the cave. The continental climatic environment inside the cave provides a possible breeding site of the potential vector. Based on the occurrence of autochthonous human cases in Thailand and on the presence of the Leishmania siamensis, it is possible that S.gemmea phlebotomine sand fly might be involved in the cycle of leishmaniasis in Thailand. The study of population activity pattern might be helpful in the implementation of successful tactics for vector control and disease prevention. ACKNOWLEDGEMENTS This study was conducted under the financial support of Naresuan University, Phitsanulok Province, Thailand. We would like to thank the staff at Khao Pattawee, Thap Than District, Uthai Thani Province for their kind cooperation during the field study; Mr Banjong Deelua and staff for the collection of specimens; and Professor Gavin Reynolds for assistance with the editing of this paper. REFERENCES Alexander B, Maroli M. Control of Phlebotomine sand flies. Med Vet Entomol 2003; 17: Apiwathnasorn C, Sucharit S, Rongsriyam Y, et al. A brief survey of Phlebotominae sand flies in Thailand. Southeast Asian J Trop Med Public Health 1989; 20: Apiwathnasorn C, Sucharit S, Surathi K, Deesin T. Anthropophilic and zoophilic phlebotomine sand flies (Diptera:Psychodidae) from Thailand. J Am Mosq Control Assoc 1993; 9: Apiwathnasorn C, Samung Y, Prummongkol S, Phayakaphon A, Panasopolkul C. Cavernicolous species of Phlebotomine sand flies from Kanchanaburi province, with an update species list for Thailand. Southeast Asian J Trop Med Public Health 2011; 42: Azizi K, Rassi Y, Javadian E, et al. First detection of Leishmania infantum in Phlebotomus Vol 46 No. 3 May

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J Mukhopadhyay/*, KN Ghosh /*/+ Mem lnst Oswaldo Cruz, Rio de Janeiro, Vol. 92(l): 57-61, JanJFeb. 1997 57 Diagnostic Importance of Female External Genital Structure of Phlebotomine Sand Flies (Diptera:Psychodidae) as Observed by Scanning